Cargando…
Evolution of biofilm-forming pathogenic bacteria in the presence of nanoparticles and antibiotic: adaptation phenomena and cross-resistance
BACKGROUND: Treatment of bacterial biofilms are difficult and in many cases, expensive. Bacterial biofilms are naturally more resilient to antimicrobial agents than their free-living planktonic counterparts, rendering the community growth harder to control. The present work described the risks of lo...
Autores principales: | , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2021
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8474960/ https://www.ncbi.nlm.nih.gov/pubmed/34579731 http://dx.doi.org/10.1186/s12951-021-01027-8 |
_version_ | 1784575339823890432 |
---|---|
author | Mann, Riti Holmes, Amy McNeilly, Oliver Cavaliere, Rosalia Sotiriou, Georgios A. Rice, Scott A. Gunawan, Cindy |
author_facet | Mann, Riti Holmes, Amy McNeilly, Oliver Cavaliere, Rosalia Sotiriou, Georgios A. Rice, Scott A. Gunawan, Cindy |
author_sort | Mann, Riti |
collection | PubMed |
description | BACKGROUND: Treatment of bacterial biofilms are difficult and in many cases, expensive. Bacterial biofilms are naturally more resilient to antimicrobial agents than their free-living planktonic counterparts, rendering the community growth harder to control. The present work described the risks of long-term use of an important alternative antimicrobial, silver nanoparticles (NAg), for the first time, on the dominant mode of bacterial growth. RESULTS: NAg could inhibit the formation as well as eradicating an already grown biofilm of Pseudomonas aeruginosa, a pathogen notorious for its resilience to antibiotics. The biofilm-forming bacterium however, evolved a reduced sensitivity to the nanoparticle. Evidence suggests that survival is linked to the development of persister cells within the population. A similar adaptation was also seen upon prolonged exposures to ionic silver (Ag(+)). The persister population resumed normal growth after subsequent passage in the absence of silver, highlighting the potential risks of recurrent infections with long-term NAg (and Ag(+)) treatments of biofilm growth. The present study further observed a potential silver/antibiotic cross-resistance, whereby NAg (as well as Ag(+)) could not eradicate an already growing gentamicin-resistant P. aeruginosa biofilm. The phenomena is thought to result from the hindered biofilm penetration of the silver species. In contrast, both silver formulations inhibited biofilm formation of the resistant strain, presenting a promising avenue for the control of biofilm-forming antibiotic-resistant bacteria. CONCLUSION: The findings signify the importance to study the nanoparticle adaptation phenomena in the biofilm mode of bacterial growth, which are apparently unique to those already reported with the planktonic growth counterparts. This work sets the foundation for future studies in other globally significant bacterial pathogens when present as biofilms. Scientifically based strategies for management of pathogenic growth is necessary, particularly in this era of increasing antibiotic resistance. GRAPHIC ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12951-021-01027-8. |
format | Online Article Text |
id | pubmed-8474960 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-84749602021-09-28 Evolution of biofilm-forming pathogenic bacteria in the presence of nanoparticles and antibiotic: adaptation phenomena and cross-resistance Mann, Riti Holmes, Amy McNeilly, Oliver Cavaliere, Rosalia Sotiriou, Georgios A. Rice, Scott A. Gunawan, Cindy J Nanobiotechnology Research BACKGROUND: Treatment of bacterial biofilms are difficult and in many cases, expensive. Bacterial biofilms are naturally more resilient to antimicrobial agents than their free-living planktonic counterparts, rendering the community growth harder to control. The present work described the risks of long-term use of an important alternative antimicrobial, silver nanoparticles (NAg), for the first time, on the dominant mode of bacterial growth. RESULTS: NAg could inhibit the formation as well as eradicating an already grown biofilm of Pseudomonas aeruginosa, a pathogen notorious for its resilience to antibiotics. The biofilm-forming bacterium however, evolved a reduced sensitivity to the nanoparticle. Evidence suggests that survival is linked to the development of persister cells within the population. A similar adaptation was also seen upon prolonged exposures to ionic silver (Ag(+)). The persister population resumed normal growth after subsequent passage in the absence of silver, highlighting the potential risks of recurrent infections with long-term NAg (and Ag(+)) treatments of biofilm growth. The present study further observed a potential silver/antibiotic cross-resistance, whereby NAg (as well as Ag(+)) could not eradicate an already growing gentamicin-resistant P. aeruginosa biofilm. The phenomena is thought to result from the hindered biofilm penetration of the silver species. In contrast, both silver formulations inhibited biofilm formation of the resistant strain, presenting a promising avenue for the control of biofilm-forming antibiotic-resistant bacteria. CONCLUSION: The findings signify the importance to study the nanoparticle adaptation phenomena in the biofilm mode of bacterial growth, which are apparently unique to those already reported with the planktonic growth counterparts. This work sets the foundation for future studies in other globally significant bacterial pathogens when present as biofilms. Scientifically based strategies for management of pathogenic growth is necessary, particularly in this era of increasing antibiotic resistance. GRAPHIC ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12951-021-01027-8. BioMed Central 2021-09-27 /pmc/articles/PMC8474960/ /pubmed/34579731 http://dx.doi.org/10.1186/s12951-021-01027-8 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Mann, Riti Holmes, Amy McNeilly, Oliver Cavaliere, Rosalia Sotiriou, Georgios A. Rice, Scott A. Gunawan, Cindy Evolution of biofilm-forming pathogenic bacteria in the presence of nanoparticles and antibiotic: adaptation phenomena and cross-resistance |
title | Evolution of biofilm-forming pathogenic bacteria in the presence of nanoparticles and antibiotic: adaptation phenomena and cross-resistance |
title_full | Evolution of biofilm-forming pathogenic bacteria in the presence of nanoparticles and antibiotic: adaptation phenomena and cross-resistance |
title_fullStr | Evolution of biofilm-forming pathogenic bacteria in the presence of nanoparticles and antibiotic: adaptation phenomena and cross-resistance |
title_full_unstemmed | Evolution of biofilm-forming pathogenic bacteria in the presence of nanoparticles and antibiotic: adaptation phenomena and cross-resistance |
title_short | Evolution of biofilm-forming pathogenic bacteria in the presence of nanoparticles and antibiotic: adaptation phenomena and cross-resistance |
title_sort | evolution of biofilm-forming pathogenic bacteria in the presence of nanoparticles and antibiotic: adaptation phenomena and cross-resistance |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8474960/ https://www.ncbi.nlm.nih.gov/pubmed/34579731 http://dx.doi.org/10.1186/s12951-021-01027-8 |
work_keys_str_mv | AT mannriti evolutionofbiofilmformingpathogenicbacteriainthepresenceofnanoparticlesandantibioticadaptationphenomenaandcrossresistance AT holmesamy evolutionofbiofilmformingpathogenicbacteriainthepresenceofnanoparticlesandantibioticadaptationphenomenaandcrossresistance AT mcneillyoliver evolutionofbiofilmformingpathogenicbacteriainthepresenceofnanoparticlesandantibioticadaptationphenomenaandcrossresistance AT cavaliererosalia evolutionofbiofilmformingpathogenicbacteriainthepresenceofnanoparticlesandantibioticadaptationphenomenaandcrossresistance AT sotiriougeorgiosa evolutionofbiofilmformingpathogenicbacteriainthepresenceofnanoparticlesandantibioticadaptationphenomenaandcrossresistance AT ricescotta evolutionofbiofilmformingpathogenicbacteriainthepresenceofnanoparticlesandantibioticadaptationphenomenaandcrossresistance AT gunawancindy evolutionofbiofilmformingpathogenicbacteriainthepresenceofnanoparticlesandantibioticadaptationphenomenaandcrossresistance |